In theory, evolutionary modularity allows anatomical structures to respond differently to selective regimes, thus promoting morphological diversification. These differences can then influence the rate and direction of phenotypic evolution among structures. Here we use geometric morphometrics and phenotypic matrix statistics to compare rates of craniofacial evolution and estimate evolvability in the face and braincase modules of a clade of teleost fishes (Gymnotiformes) and a clade of mammals (Carnivora), both of which exhibit substantial craniofacial diversity. We find that the face and braincase regions of both clades display different degrees of integration. We find that the face and braincase evolve at similar rates in Gymnotiformes and the reverse in Carnivora with the braincase evolving twice as fast as the face. Estimates of evolvability and constraints in these modules suggest differential responses to selection arising from fluctuations in phylogenetic integration, thus influencing differential rates of skull-shape evolution in these two clades.
Although rare within the context of 30 000 species of extant fishes, scale-feeding as an ecological strategy has evolved repeatedly across the teleost tree of life. Scale-feeding (lepidophagous) fishes are diverse in terms of their ecology, behaviour, and specialized morphologies for grazing on scales and mucus of sympatric species. Despite this diversity, the underlying ontogenetic changes in functional and biomechanical properties of associated feeding morphologies in lepidophagous fishes are less understood. We examined the ontogeny of feeding mechanics in two evolutionary lineages of scale-feeding fishes: Roeboides, a characin, and Catoprion, a piranha. We compare these two scale-feeding taxa with their nearest, non-lepidophagous taxa to identify traits held in common among scale-feeding fishes. We use a combination of micro-computed tomography scanning and iodine staining to measure biomechanical predictors of feeding behaviour such as tooth shape, jaw lever mechanics and jaw musculature. We recover a stark contrast between the feeding morphology of scale-feeding and non-scale-feeding taxa, with lepidophagous fishes displaying some paedomorphic characters through to adulthood. Few traits are shared between lepidophagous characins and piranhas, except for their highly-modified, stout dentition. Given such variability in development, morphology and behaviour, ecological diversity within lepidophagous fishes has been underestimated.
Convergent evolution is widely viewed as strong evidence for the influence of natural selection on the origin of phenotypic design. However, the emerging evo‐devo synthesis has highlighted other processes that may bias and direct phenotypic evolution in the presence of environmental and genetic variation. Developmental biases on the production of phenotypic variation may channel the evolution of convergent forms by limiting the range of phenotypes produced during ontogeny. Here, we study the evolution and convergence of brachycephalic and dolichocephalic skull shapes among 133 species of Neotropical electric fishes (Gymnotiformes: Teleostei) and identify potential developmental biases on phenotypic evolution. We plot the ontogenetic trajectories of neurocranial phenotypes in 17 species and document developmental modularity between the face and braincase regions of the skull. We recover a significant relationship between developmental covariation and relative skull length and a significant relationship between developmental covariation and ontogenetic disparity. We demonstrate that modularity and integration bias the production of phenotypes along the brachycephalic and dolichocephalic skull axis and contribute to multiple, independent evolutionary transformations to highly brachycephalic and dolichocephalic skull morphologies.
Evolutionary innovations are scattered throughout the tree of life, and have allowed the organisms that possess them to occupy novel adaptive zones. While the impacts of these innovations are well documented, much less is known about how these innovations arise in the first place. Patterns of covariation among traits across macroevolutionary time can offer insights into the generation of innovation. However, to date, there is no consensus on the role that trait covariation plays in this process. The evolution of cranial asymmetry in flatfishes (Pleuronectiformes) from within Carangaria was a rapid evolutionary innovation that preceded the colonization of benthic aquatic habitats by this clade, and resulted in one of the most bizarre body plans observed among extant vertebrates. Here, we use three-dimensional geometric morphometrics and a phylogenetic comparative toolkit to reconstruct the evolution of skull shape in carangarians, and quantify patterns of integration and modularity across the skull. We find that the evolution of asymmetry in flatfishes was a rapid process, resulting in the colonization of novel trait space, that was aided by strong integration that coordinated shape changes across the skull. Our findings suggest that integration plays a major role in the evolution of innovation by synchronizing responses to selective pressures across the organism.
Abstract.—Modularity is a ubiquitous feature of organismal design that plays an important role in structuring patterns of morphological diversification. Modularity can facilitate evolutionary changes by allowing subsets of traits to coevolve as integrated units and follow quasi-independent evolutionary trajectories, a pattern that may be particularly consequential in the case of highly complex morphological structures. Here we examine modularity in a complex and highly kinetic structure, the teleost skull, and ask if a modular organization of the skull has influenced the diversification dynamics of the shapes of its osteological components across the labrid phylogeny. We compiled one of the largest 3D morphological data sets of fishes to date and used geometric morphometrics to quantify patterns of cranial shape evolution across 184 species of wrasses (Labridae). We then tested several hypotheses of modularity inspired by functional and developmental relationships between cranial bones and compared phenotypic rates among modules. We also compared the fit of models of trait evolution for the entire skull and the various articulated bones that it comprises. Our analyses indicated strong support for a 2-module hypothesis, one that encompasses the oral and pharyngeal jaws and another module comprised of the neurocranium, hyoid apparatus, and operculum. This functional hypothesis yielded one of the highest significant rate differentials across modules, yet we also found that the best-fitting models of trait evolution differed among skull bones. These results suggest that modularity can influence morphological diversification in complex biological structures via differences in both the tempo and mode of evolutionary change. [3D geometric morphometrics, cranial morphology, evolutionary modularity, Labridae, phenotypic rates, structural complexity.]
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